Mediterranean vineyards and olive groves in Croatia harbour some rare and endemic invertebrates

Biodiversity Data Journal 11: e100963 'e @)
doi: 10.3897/BDJ.11.e100963 open access
Research Article

Mediterranean vineyards and olive groves in
Croatia harbour some rare and endemic
invertebrates

Barbara Andelié Dmitrovic?, Lara lvankovié Tatalovi¢?, Tomislav KosS, Petar Crnéan!, Domagoj Gajski,
Migel Jelic*, Lucija Serié Jelaskat

+ Department of Biology, Faculty of Science, University of Zagreb, Rooseveltov trg 6, Zagreb, Croatia

§ Department for Ecology, Agronomy and Aquaculture, University of Zadar, Trg kneza ViSeslava, Zadar, Croatia

| Croatian Natural History Museum, Demetrova 1, Zagreb, Croatia

4 Department of Botany and Zoology, Faculty of Science, Masaryk University, Kotlarska 2, Brno, Czech Republic
# Varazdin City Museum, Setali8te Josipa Jurja Strossmayera 3, VarazZdin, Croatia

Corresponding author: Lara lvankovié Tatalovié (lara.ivankovic@biol.pmf.hr), Lucija Serié Jelaska
(slucija@pbiol.pmf.hr)

Academic editor: Dimitris Poursanidis
Received: 24 Jan 2023 | Accepted: 05 Mar 2023 | Published: 20 Apr 2023

Citation: Andelié Dmitrovié B, Ivankovié Tatalovié L, Kos T, Crnéan P, Gajski D, Jelié M, Serié Jelaska L (2023)
Mediterranean vineyards and olive groves in Croatia harbour some rare and endemic invertebrates. Biodiversity
Data Journal 11: e€100963. https://doi.org/10.3897/BDJ.11.e100963

Abstract

The Mediterranean is characterised by high biodiversity and numerous endemic species.
These species are not only present in natural habitats, but also inhabit areas under human
influence, such as agricultural lands. In the biodiversity assessment of Mediterranean
vineyards and olive orchards within Zadar County, in Croatia, we identified eight endemic
species with Mediterranean distribution, six with a Balkan Peninsula distribution, four with
Dinaric Alps distribution and three species rare and endangered in Europe. Alongside
these species, we have recorded five new species for Croatian fauna, many of those
identified by combining morphological characteristics and the DNA barcoding tool. Araneae
and Coleoptera contributed the highest number of endemic species and groups with new
record were the following: Coleoptera, Diptera and Araneae. Compared to other sites, an
olive orchard with ecological pest management (EPM), surrounded by natural ecosystems,
had the highest ratio of endemic and rare species. Our findings emphasise that agricultural
lands in the Mediterranean can be habitats for endemic and rare species and that future

© Andeli¢ Dmitrovié B et al. This is an open access article distributed under the terms of the Creative Commons Attribution
License (CC BY 4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author
and source are credited.

2 Andelié Dmitrovié B et al

biodiversity research of these habitats is highly important, to monitor potential biodiversity
changes and motivate future species and ecosystem conservation.

Keywords

Araneae, Balkan Penninsula, carabids, endemics, gastropoda, Mediterranean, endangered
species

Introduction

The coastal part of Croatia, which is situated in the wider Mediterranean region and Balkan
Peninsula, has high biodiversity and numerous endemic species (Jelaska et al. 2010). The
Mediterranean Region, including the Balkan Peninsula, has high non-marine molluscs
diversity and is rich in endemic species (Cuttelod et al. 2011). The Balkan Peninsula and
its neighbouring islands are amongst the world's areas with the greatest concentration of
terrestrial slugs. There are 101 species of Arionidae, Milacidae, Limacidae and
Agriolimacidae in this small area. The vast majority, or 66%, are endemic species with
typically relatively small ranges (Wiktor 1997). According to Stamol et al. (2017), there are
328 species and 203 subspecies of land snails inhabiting Croatia. Endemics make a
significant part of this malacofauna - 15% of valid species and 46% of valid subspecies are
Croatian endemics. Furthermore, both at genus and species level, spiders (Araneae) are
another arthropod group that is highly diverse in this area, with numerous endemics within
the Balkan Peninsula (Griffiths et al. 2004). Deltshev (1999) identified Croatia as the
Balkan Peninsula's country with the second highest number of endemic spider species
after Greece. Croatia has 30 endemic spider species, while there are another 31 native to
the Balkan Peninsula (Katusic 2017). In terms of insect diversity, Croatia is amongst the
richest European countries for Orthopterans (Skejo et al. 2018). Orthopterans are
frequently considered significant contributors to farmland biodiversity (Ichihara et al. 2015)
and, because the Mediterranean shrubland is especially rich in species, there is a belief
that traditional agricultural landscapes have a positive role in keeping the biodiversity of
these insects high (Hochkirch 2016). Many orthopteran species and subspecies are
present and even recently discovered (Ciplak et al. 2007). Endemic, rare and endangered
species of carabid beetles are published within the Red List for Croatia (Vujcic-Karlo et al.
2007) and some of these species are known to appear in the Mediterranean part of the
country (Rukavina et al. 2010). Within the genus Carabus, there are several endangered
and endemic species with a narrow distribution area that encompasses Croatia and
neighbouring Bosnia and Hercegovina (Seri¢é Jelaska et al. 2004, Jambrogié Viadié and
Seri¢é Jelaska 2020, Jambrosi¢ Vladi¢ 2020). For some groups, there is a lack of
knowledge on their distribution and ecology which complicates evaluation of endemic
species. This applies to the Croatian ant fauna, whose biodiversity is understudied.
Considering that part of Croatia is situated in the Mediterranean Region, which has
Europe's richest ant fauna, the number of reported ant species is projected to be larger in
the Mediterranean part of Croatia in comparison to other parts of the country (Bracko and
G 2006). Half of the Croatian ant species have a Mediterranean distribution, i.e. those that

Mediterranean vineyards and olive groves in Croatia harbour some rare and ... 3

are commonly found in the Mediterranean Region (Bracko and G 2006). Species of Diptera
and Hemiptera in agricultural lands have wide geographical distribution and are mainly
influenced by the crop type (Franin et al. 2021). In this area, wine and olive oil production
has a long history and vineyards and olive groves are common parts of the landscape
(Froidevaux et al. 2017). Intensive agriculture is considered as a threat to biodiversity
alongside other human interventions to the landscape (Ricketts and Imhoff 2003). The
main threat of agricultural production to the ecosystem lies in the application of pesticides,
mainly insecticides, then chemical fertilisers, with lack of organic matter in soils, but also in
the heavy disturbance of the upper soil layers by machinery. Numerous research studies
showed negative impacts of pesticide application to the non-target invertebrates in the
agricultural ecological systems (Moreby et al. 1997, Pisa et al. 2015, lvankovic Tatalovic et
al. 2020) with a high negative impact on soil organisms (Gunstone et al. 2021). In this area,
wine and olive oil production has a long history and vineyards and olive groves been
common parts of the landscape (Froidevaux et al. 2017, Kavvadias and Koubouris 2019).
Intensive agriculture is considered as a threat to biodiversity alongside other human
interventions to the landscape (Ricketts and Imhoff 2003). The main of them lies in the
application of pesticides, mainly insecticides, then chemical fertilisers. According to Baric
and Pajaé Zivkovic (2020), IPM have wider aims to benefit human and environmental
health and to sustain economically balanced agricultural production. The EPM on the other
hand is, in the context of agricultural production, an even higher approach in pest
management because it reduces to a minimum or excludes the use of synthetic pesticides
and fertilisers in general (EC 889/2008), with the aim to benefit agriculture sustainability
even more than IPM. Increasing implementation of biological approaches, including
biological control, biopesticides, biostimulants and pheromones is a mutually high priority
for sustainable agriculture leaders and practitioners, including those working in organic
agriculture and IPM (Baker et al. 2020). Research shows that IPM and EPM do not
necessarily negatively affect predatory arthropods, carabid beetles and spiders (Bahlai et
al. 2010). Serié Jelaska et al. (2022b) results show that management affects the
composition of the carabids community in terms of predator share and functional diversity
(relative to control), but there are no significant differences between the two types of
management, IPM and EPM.

This paper aimed to identify rare and endemic invertebrate species in agricultural
landscapes as a part of biodiversity assay and to analyse the proportion of endemics within
vine and olive groves in Zadar County in Croatia. Fauna of rare, endemic and newly-
recorded species were presented for the following invertebrate groups: Gastropoda,
Araneae (Arahnida) and Insects - Diptera, Coleoptera, Hemiptera, Hymenoptera. The
emphasis was given to predator groups Araneae (Arahnida) and Carabidae (Coleoptera,
Insecta).

4 Andelié Dmitrovié B et al

Materials and methods
Study sites and sample collection

Studied vineyards and olive groves were situated in Zadar County, in the south of Croatia
(Fig. 1). Two sites were within olive orchards, respectively with ecological (OE) and
integrated (IO) management and two sites were placed within vineyards with the same
management types, ecological (VE) and integrated (VI). Details on agricultural practices
applied on these sites are given in Table 1 and Fig. 2. The study locations were in the
K6ppen climate classification's Mediterranean climatic types (Csa), with wet, mild winters
and dry, hot summers (Bolle 2003). Sampling was done in two years, 2018 and 2019, in
spring and autumn. The collection periods were in both 2018 and 2019 from April to July
and from September to November. Four sampling methods were used: pitfall traps, beating
stick with a net method (Schowalter and Chao 2021), Tullgren Funnel method (Macfadyen
1953) and hand picking (Table 2). The first collection method was sampling with pitfall traps
(8 cm @, volume 300 ml) during the season in 2018. Altogether, 12 traps per site were used
and placed parallel within the plantation, with the approximate space between the traps of
10 up to 12 m. Traps were buried directly under the olive trees or under the grapevine
stumps. Beating stick with a net method was solely applied in vineyards and olive orchards
in 2018. The sampling effort was unique during the season and involved hits on five
branches on twelve different trees. Sampling of the soil for the Tullgren Funnel method was
done once in April and once in October in 2018 at 12 sampling points per site, with 3 litres
of the upper 10 cm soil layer being collected.

327339 377389 427369 4773539

4910485

488985

48 TU4ES

Figure 1. EESl

Map of Zadar County, Croatia with four study sites (Transverse Mercator Projection, HTRS96/
TM): (1) a vineyard with IPM (located in BaStica); (2) an olive orchard with IPM (located in
Skabrnja); (3) a vineyard with EPM (located in Nadin); (4) an olive orchard with EPM (located
in Poli¢nik).

Mediterranean vineyards and olive groves in Croatia harbour some rare and ...

Table 1.

The list of study sites with additional information on location of the site, abbreviation, pest
management type applied on the site, size of the area, vegetation and weed processing and soil
processing in the terms of mulching, ploughing and number of pesticides treatment. Added
pesticides have been grouped according to the main active compounds, those being synthetic
(Organochlorides and chlorinated hydrocarbons, Organophosphates, Pyrethroids, Neonicotinoids
and Ryanoids), biological (Bt kurstaki, Spinosad) and copper ones (Copper(l) oxide or copper
oxychloride).

Type of
Study

Site

Olive

orchard

Vineyard

Location

Poli¢nik, OE

Zadar
County,

Croatia

Skabrnja, O
Zadar
County,

Croatia

Nadin, VE

Zadar
County,

Croatia

Ba&stica, Vi
Zadar
County,

Croatia

Table 2.

Total number of identified species per taxonomic group and per sampling method used. Number
zero (0) indicates that no specimens were caught by the method, while dash (/) indicates that
specimens were caught, but not identified to the species level.

Taxon

Gastropoda
Araneae
Orthoptera

Carabidae

Abbreviation Pest

Management

Type

ecological

integrated

ecological

integrated

Area

(ha)

24

0,85

15

Vegetation and
weed

procession

Rocky soil with
little plant
coverage and

regular mowing

Grass coverage,

surrounded by
coppice, and

regular mowing

Tilled soil with

weeds

Tilled soil with

weeds

Mulching Ploughing Synthetic

Yes

Yes

Yes

Yes

Number of species per sampling method

Pitfall traps

pesticides*
No 0
No 6
Yes 0
Yes 12

Biological

pesticides**

Beating stick | By hand

/ / 0
30 7 0
11 0 0
0 24 0

Copper

compounds

Tullgren funel

6 Andelié Dmitrovié B et al

Taxon Number of species per sampling method
Pitfall traps Beating stick By hand Tullgren funel
Other Coleoptera / 0 8 0
Hymenoptera 5 11 3 1
Hemiptera / 15 7 0
Diptera / 14 2 0
14000 -
cy copper
= 12000 + $
~ gliphosate
=]
2. 10000 - thiam etoxam
= : :
= 3000 - cihalotrin
3 w dim etoat
vu |
i” = eens
S 4000 - ® cyprodinil
5 ®™ quinox yfen
2 2000 a
= ® tebuconazole
0+ ' cyflufenam id
VI Ol VE OE = fosetil
Figure 2. EES

The amount of pesticides added at each study site during 2018, shown as grams of active
substances applied per hectare. For site abbreviations, see Table 1.

Morphological identification and DNA barcoding

Gastropods were identified using the key of Welter-Schultes (2012). Spiders collected by
pitfall traps method were classified to species or genus level following araneae - Spiders of
Europe site (https://www.araneae.nmbe.ch, accessed on 23 March 2022) (Nentwig 2022).
Orthopteran specimens were collected using beating method and pitfall traps and identified
using Harz (1969). Carabid beetles collected by pitfall traps were isolated and identified to
species following taxonomic keys by Trautner and Geigenmiller (1987), Hurka (1996) and
Freude et al. (2004) and the Fauna Europaea nomenclature (Vigna Taglianti 2013). For ant
species determination, two keys were used, Seifert (2018) and Lebas et al. (2019) and the
AntWeb website (https//:www.antweb.org, accessed on 23 March 2022) (California
Academy of Science 2002). For Hemipteran and Dipteran species or morpho-species
identification, a photographic guide to Insects of Southern Europe and the Mediterranean
was used (Brock 2017).

Species pertaining to the following groups: Araneae and Coleoptera; Carabidae and
Chrysomelidae, Hymenoptera; Formicidae, Hemiptera, Diptera, were collected using

Mediterranean vineyards and olive groves in Croatia harbour some rare and ... 7

beating stick with a net method, Tullgren Funnel method and by hand were analysed using
the integrative taxonomy approach, combining morphological identification using the
above-mentioned taxonomic keys and the DNA barcoding method. Total genomic DNA
isolation, PCR amplification, amplicon purification, sequencing and genetic data analysis
were performed as described in Andelic Dmitrovic et al. (2022). Individuals identified by the
DNA barcoding method are available in the Barcode of Life Database (BOLD)
(Ratnasingham and Hebert 2007).

Data analysis

The information on species distribution was obtained from the following bases: Fauna
Europaea (De Jong et al. 2014), Global Biodiversity Information Facility (GBIF) (GBIF org.
2022), MolluscaBase (httos:/Avww.molluscabase.org, accessed on 4 February 2022)
(MolluscaBase Eds. 2022), araneae - Spiders of Europe (Nentwig 2022), Orthoptera
Species File Version 5.0/5.0 (Cigliano et al. 2022), Barcode of Life Data system (BOLD)
(Ratnasingham and Hebert 2007, Ratnasingham and Hebert 2013), PESI database (http://
www.eu-nomen.eu/ portal/, accessed on 12 May 2022) (de Jong et al. 2015), True hoppers
WP database (hitps:/Awww.truehopperswp.com/, accessed on 12 May 2022), BioLib
database (htips:// www.biolib.cz/en/main/, accessed on 12 May 2022), The IUCN Red List
of Threatened Species (https://www.iucnredlist.org/, accessed on 12 May 2022) and FLOW
database (Bourgoin and T 2022). The species was listed as endemic with the
Mediterranean, Balkan Peninsula or Dinaric Alps distribution only in cases when all data on
distribution were in consent. The list of rare and endangered species, amongst all species
recorded at studied sites, was obtained using the Red List in the case of carabid beetles
(Vujcic-Karlo et al. 2007), araneae - Spiders of Europe site and communication with
experts in the case of spiders. Other groups that contain endemic species were also
verified for existence of rare and new species for Croatia through correspondence with
taxonomic experts and available data in the above-mentioned databases and current
papers (Kuntner 1997, Bracko and G 2006, Borowiec and Salata 2012, Borowiec 2014,
Gnezdilov et al. 2014, Skejo et al. 2018, Grbac et al. 2019).

Evenness, as well as Shannon, Simpson and Margalef diversity indices were calculated in
PAST 4.03 (Hammer et al. 2001, Happe et al. 2019), for Gastropoda, Araneae and
Coleoptera, as these groups were regularly collected across seasons using the pitfall trap
method and all specimens pertaining to these groups were identified to species by
taxonomic experts.

A Venn diagram, depicting number of species per sampling method, was plotted using
online software at https://bioinformatics.psb.ugent.be/webtools/Venn/ (accessed on 25
March 2022).

8 Andelié Dmitrovié B et al

Results
Endemic, rare and species new to Croatia

Altogether, 280 species of Gastropoda, Araneae, Orthoptera, Coleoptera, Hymenoptera,
Hemiptera and Diptera were collected using all sampling methods and the total list of all
recorded invertebrate species at five sites is published in GBIF database (Seri¢ Jelaska et
al. 2022a). Pitfall traps yielded most species, followed by the beating stick with a net and
hand picking. Only one ant species was collected using the Tullgren funnel (Fig. 3).

Pitfall trap By hand

Beating stick

Figure 3. EES]

Venn diagram depicting the number of all collected species per sampling method.

Of the invertebrate fauna collected in vineyards and olive orchards in Zadar County,
spiders contributed with the highest number of endemic species, six, distributed either in
the Mediterranean Region or in the Dinaric Alps (Table 3). In addition, five endemic carabid
beetles were collected; three of which are distributed in the Balkan Peninsula and two in
the Mediterranean. In the case of Gastropoda species, Delima semirugata is endemic to
Croatia and Montenegro and Tandonia reuleauxi is endemic to the western Balkan
Peninsula and Italy (Bank and Neubert 2020). Additionally, two spider species, Attu/us
penicillatus and Zelotes hermani, are described as very rarely found on the Spiders of
Europe site. Orthopterans Ephippiger discoidalis, Barbitistes yersini and Eupholidoptera
schmidti are endemic to the Balkan Peninsula and Italy. Besides these groups, one
hemipteran (Latissus dilatatus) and one hymenopteran (Aphaenogaster picena) endemic
species with a Mediterranean distribution were recorded in the study area. Furthermore,
the collected species Ditomus calydonius, while not considered as an endemic species, is
listed on the carabid beetles Red List of Croatia (Vujcic-Karlo et al. 2007) as a critically
endangered species. Out of 280 (Seri¢ Jelaska et al. 2022a) recorded species at our study
sites, collected and identified using the above-mentioned methods, five had no previous
records for Croatia. Those are, Ceratinella brevipes (Westring, 1851) (Araneae,
Lyniphiidae) (Suppl. material 1), one male specimen collected in vineyard with IPM;

Mediterranean vineyards and olive groves in Croatia harbour some rare and ... FS)

Anthomyia liturata (Robineau-Desvoidy, 1830) (Diptera, Tabanidae) (BOLD:ACE4540)
(Suppl. material 2), one specimen recorded in vineyard with IPM; Corynoptera perpusilla
Winnertz, 1867 (Diptera, Sciaridae) (BOLD:AAN6447) (Suppl. material 3), one specimen
recorded in olive orchard with IPM; Psilopa obscuripes Loew, 1860 (Diptera, Ephydridae)
(BOLD:AAG7016) (Suppl. material 4), 11 specimens recorded in vineyard with IPM;
Aphthona pallida (Bach, 1856) (Coleoptera, Chrysomelidae) (BOLD:ACZ1493) and one
specimen recorded in olive orchard with EPM. The endemic and rare species and those
new to Croatia have been listed in the Table 3.

Table 3.

List of endemic, rare and endangered species collected in all four sampling sites. M — species with
the area limited to the Mediterranean Region; D — species with the area limited to the region of the
Dinaric Alps; B — species with the area limited to the Balkan Peninsula.

Class Order Family Species Endemics Rare and/or New
endangered records
species for

Croatia

Gastropoda Stylommatophora Clausiliidae Delima semirugata B

(Rossmassler, 1836)

Stylommatophora Milacidae Tandonia reuleauxi B
(Clessin, 1887)

Arachnida Araneae Thomisidae Bassaniodes bufo M
(Dufour, 1820)

Araneae Salticidae Attulus penicillatus ‘
(Simon, 1875)

Araneae Lyniphiidae Ceratinella brevipes %
(Westring, 1851)

Araneae Gnaphosidae Zelotes hermani *
(Chyzer, 1897)

Araneae Gnaphosidae Marinarozelotes M
holosericeus (Simon,
1878)

Araneae Philodromidae Pulchellodromus M
bistigma (Simon,
1870)

Araneae Agelenidae Urocoras munieri D
(Simon, 1880)

Araneae Thomisidae Xysticus apricus L. D
Koch, 1876

10

Class

Insecta

Order

Araneae

Diptera

Diptera

Diptera

Coleoptera

Coleoptera

Coleoptera

Coleoptera

Coleoptera

Coleoptera

Coleoptera

Hemiptera

Hymenoptera

Orthoptera

Andelié Dmitrovié B et al

Family Species Endemics Rare and/or
endangered
species

Zodariidae Zodarion elegans M

(Simon, 1873)
Tabanidae Anthomyia liturata
(Robineau-Desvoidy,
1830)

Sciaridae Corynoptera
perpusilla Winnertz,
1867

Ephydridae Psilopa obscuripes
Loew, 1860

Carabidae Carabus caelatus B

dalmatinus

Duftschmid, 1812
Chrysomelidae Aphthona pallida

(Bach, 1856)

Carabidae Carabus coriaceus B

dalmaticus Géhin,
1885
Carabidae Zabrus incrassatus B
(Ahrens, 1814)
Carabidae Amara dalmatina M
Dejean, 1828
Carabidae Ditomus calydonius ‘
P. Rossi, 1790
Carabidae Olisthopus fuscatus M

Dejean, 1828

Issidae Latissus dilatatus M
(Fourcroy, 1785)

Formicidae Aphaenogaster D
picena Baroni Urbani,
1971

Tettigoniidae § Ephippiger D
discoidalis Fieber,
1853

New
records
for

Croatia

Mediterranean vineyards and olive groves in Croatia harbour some rare and ... 11

Class Order Family Species Endemics Rare and/or New
endangered records
species for

Croatia
Orthoptera Tettigoniidae | Eupholidoptera B
schmidti (Fieber,
1861)
Orthoptera Tettigoniidae Barbitistes yersini M

Brunner von
Wattenwyl, 1878

The ratio of endemic, rare and newly-recorded species within Gastropoda, Araneae and
Carabidae, comparing to those with wider distribution, is shown in Fig. 4. In the case of
Araneae species, endemic and rare species accounted for 7% of the total number of
species found. In the Carabidae family, endemics and rare species accounted for 8% of
total species, while in Gastropoda, they accounted for 16%.

a)

b) c)

Endemics ® Rare and endangerd species (not endemic) = Other species

Figure 4. EES]

Ratio of endemic and rare to globally distributed spiders (a), carabid beetles (b) and
gastropods (c) analysed for all the sites together.

Comparison of newly-recorded, endemic and rare species distribution amongst our
sampling sites showed that, overall, olive orchards with EPM harboured the highest share
of endemic species, but not individuals pertaining to these species (Fig. 5). However, the
highest abundance and the highest number of newly-recorded species was observed for
vineyards with IPM.

Diversity measures

The Shannon Diversity Index was slightly higher in EPM sites than those with IPM for
spiders, but the opposite values were for carabid beetles and gastropods. A similar trend
can be observed with Evenness and species richness shown as the Margalef Index, which
were higher in IPM than EPM sites. The higest values of diversity indices for Carabidae
and Gastropoda was observed in the olive orchard with IPM. Most of the diversity indices

12 Andeli¢ Dmitrovié B et al

measured for Aranaea species were higher in EPM sites. These results are depicted in the
Table 4.

(a)

Pitonics Rare New
species _ records
Site
oe a z | Bore
OI 75%

VE er
VI — 25%
0%

(b)|
nicenion Rare New
Site species _ records
ce iim | Barn
OI 75%
_ 50%
(il 0%
Figure 5. EES

Heat map depicting the ratio of each site in the number of endemic, rare and newly-recorded
species (a) and the abundance of the corresponding individuals (b). Study sites are denoted
with abbreviations as follows: OE - olive orchard with EPM; OI - olive orchard with IPM; VE -
vineyard with EPM; VI - vineyard with IPM.

Table 4.

Diversity indices for Araneae, Carabidae and Gastropoda collected by pitfall traps for each research
Site.

Site Taxon Shannon H Simpson 1-D Evenness e“H/S Margalef

Olive orchard with EPM Gastropoda 0.01 0 0.51 0.15
Araneae 3.54 0.96 0.63 9.87
Carabidae 1.87 0.71 0.27 4.22

Olive orchard with IPM Gastropoda 1.41 0.69 0.68 0.98
Araneae 3.29 0.93 0.33 11.72

Carabidae 2.3 0.86 0.3 4.47

Mediterranean vineyards and olive groves in Croatia harbour some rare and ... 13

Site Taxon Shannon H Simpson 1-D Evenness e“H/S Margalef
Vineyard with EPM Gastropoda 1.26 0.8 1.17 1.24
Araneae 3.53 0.95 0.69 9.27
Carabidae 2.02 0.8 0.24 3.93
Vineyard with IPM Gastropoda 1.01 0.44 0.46 1.41
Araneae 3.21 0.91 0.41 9.8
Carabidae 2.14 0.83 0.28 4.42
Discussion

The biodiversity of the Balkan Peninsula is still poorly researched, with new species and
new records to Croatia being continuously reported (e.g. Francuski et al. (2011), Previsic et
al. (2014)). We found no prior records in Croatia for five species noted in this study: one
Araneae species, three Diptera species and one Coleoptera species. Our results confirmed
that agricultural areas could harbour some rare and endemic species. We also found eight
endemics with Mediterranean distribution, six with Balkan Peninsula distribution and four
with Dinaric Alps distribution. Despite lower values of measured diversity indices, the total
number of endemic species and the abundance of rare species were the highest in olive
orchards with EPM. This can probably be explained by the fact that this site is, comparing
to the other agricultural sites studied, the only one that is surrounded by natural habitats,
which can positively impact invertebrate community in adjacent agroecosystems (Duque-
Trujillo et al. 2022). Three species are rare and endangered in Europe. All findings were
uploaded in the GBIF database (Seri¢ Jelaska et al. 2022a) as only the second contribution
from Croatia in this global database for faunal research, indicating the need for further
biodiversity research of the area, especially having in mind high diversity of fauna and high
endemism of this area. Further entries of biodiversity data of this area in the GBIF
database and similar databases will enable further meta-analyses of diversity on a larger
scale. The following is the list of interesting faunistic records:

Class Gastropoda

The Mediterranean Region, from the Iberian Peninsula to the Balkans, is the main centre of
diversity and endemism of non-marine molluscs (Cuttelod et al. 2011). Land snails can
adapt to challenging environments thanks to a variety of morphological, behavioural and
physiological responses to homoeostatic stimuli (Chukwuka et al. 2014). For gastropods,
the smallest diversity was observed in the case of olive orchards with EPM. Explanation for
this probably lies in the fact that olive orchards with EPM were under more intensive
disturbance of soil with mechanisation and this site was characterised by mostly bare soil
or with less plant coverage than olive orchards with the IPM site. This negatively impacted
gastropod biodiversity in EPM orchards compared to IPM, as most snails and slugs lay
their eggs in the ground and need plant coverage for summer aestivation (Godan 1983).

14 Andelié Dmitrovié B et al

Delima semirugata (Rossmassler, 1836) (Stylommatophora, Clausiliidae)

D. semirugata is a terrestrial gastropod endemic to Croatia and Montenegro, with Croatia
containing the type locality (MolluscaBase Eds. 2022). It is a grazer, as is characteristic to
the family Clausiliidae (MolluscaBase Eds. 2022). Genus Delima is rich in species endemic
to Croatia and/or its neighbouring countries on the Balkan Peninsula (MolluscaBase Eds.
2022). D. semirugata and its subspecies can be found on the Croatian coast and islands,
where they inhabit stony grasslands, smaller rocks and cracks (Stamol et al. 2017). In this
study, the species was found on the unmanaged habitat consisting of Mediterranean
scrubland, very close to the olive orchard with EPM. Although it was not recorded at the
agricultural land itself, this finding proves that the proximity of agricultural activity is not
necessarily detrimental to the presence of endemic species.

Tandonia reuleauxi (Clessin, 1887) (Stylommatophora Milacidae)

T. reuleauxi is endemic to the Dinaric Alps and can be found in Italy, Slovenia, Croatia,
Bosnia and Herzegovina and Montenegro (MolluscaBase Eds. 2022). The species lives in
xerophilous forests and can be found crawling on limestone rocks in shaded places. If it is
rainy, it is active in broad daylight (De Mattia and PeSic 2015).

Order Araneae

Spiders provided the highest number of endemic species in this study because of their
capacity to colonise large areas, including agricultural locations (Nyffeler and Sunderland
2003). Despite the high number of endemics with Croatian and Balkan Peninsula
distribution (Deltshev 1999), all endemic species were either ones with Mediterranean
distribution or Dinaric Alps distribution. This does not necessarily mean that these species
are not present in the area. As spiders have a wide range of ecological niches, sampling
them requires a combination of techniques and that can leave many species unidentified
due to a failure to cover a wide range of microhabitats (Cardoso et al. 2007). Thus, new
species and new records are still being described (Deltshev et al. 2022) and this study
proved that agroecosystems should not be excluded from such research. Due to their
predatory potential on pest species, spiders are essential predatory arthropods in
agricultural lands (Samiayyan 2014, Gajski and Pekar 2021). Their richness and diversity
promote biocontrol (Cuff et al. 2021). We found that the EPM system resulted in a higher
diversity of spiders than the IPM. This is in contrast to prior findings from olive grove
studies (Cardenas et al. 2006, Cardenas et al. 2015). Vineyards with EPM had a higher
Shannon and Simpson diversity of spiders than vineyards with IPM, contrary to gastropods
and carabid beetles. This could be linked with different ecology and habitat niches between
the groups. Spiders are active in canopy and not just on the soil and those species are not
directly influenced by soil disturbances with mechanisation, which was more intense in the
olive orchard with EPM.

Attulus penicillatus (Simon, 1875) (Araneae, Salticidae)

There is only ten records of A. penicillatus for Croatia, most of them from the late 19" and
early 20" century. It is possible that the species is rare in Croatia, but it could also be that it

Mediterranean vineyards and olive groves in Croatia harbour some rare and ... 15

is poorly researched in this part of the country (L. Katusic, personal communication, 15
February 2022). It is described as very rarely found on the Spiders of Europe site (Nentwig
2022). This is a globally distributed species that prefers warm places on sandy ground
(Nentwig 2022). A. penicillatus is an endangered and rare faunistic record.

Zelotes hermani (Chyzer, 1897) (Araneae, Gnaphosidae)

Z. hermani is recorded at multiple sites in the Mediterranean Region of Croatia, but always
in low numbers (L. Katusic, personal communication, 15 February 2022) and is described
as very rarely found on the Spiders of Europe site (Nentwig 2022). It has a global
distribution and can be found under stones in warm sites (Nentwig 2022). Z. hermani is an
endangered and rare faunistic record.

Bassaniodes bufo (Dufour, 1820) (Araneae, Thomisidae)

B. bufo is a species of Mediterranean distribution (Nentwig 2022) that can be found in olive
orchards (Picchi 2020) as was the case in our study, where it was sampled in olive
orchards with both EPM and IPM. The earliest record from Croatia is from the second half
of the 19!" century (Canestrini and Pavesi 1868) and since then, has been recorded at
more sites in the Mediterranean Region of Croatia, including the National Park Kornati
(Grbac et al. 2019).

Marinarozelotes holosericeus (Simon, 1878) (Araneae, Gnaphosidae)

M. holosericeus is a Mediterranean endemic, mostly distributed in the western
Mediterranean (Di Franco 1997), but it has been recorded in Croatia (Katusic 2017) and
Greece (Nentwig 2022). In our study, it was found in olive orchards with EPM.

Pulchellodromus bistigma (Simon, 1870) (Araneae, Philodromidae)

P. bistigma is a small (1.3-1.9 mm) spider with a Mediterranean distribution (Nentwig 2022
). The first record for Croatia is from the late 19"" century in Dalmatia (Gasperini 1891) and
later, it was found in Istria (Muster et al. 2007). We sampled this species in olive orchards,
which can be their habitat (Picchi 2020).

Urocoras munieri (Simon, 1880) (Araneae, Agelenidae)

The area of U. munieri is restricted to the region of Dinaric Alps (Venezia Giulia in Italy,
Slovenia and Croatia) (Nentwig 2022). The type locality is in Sibenik area, Croatia (Pantini
and Isaia 2019). In this research, U. munieri was collected at every sampling site with high
abundance, indicating that it is well adapted for life on agricultural land.

Xysticus apricus L. Koch, 1876 (Araneae, Thomisidae)

This species was recorded for Croatia for the first time by Draksic and KatuSic (2011) in the
National Park Kornati. Before that, it was endemic to Italy (Pantini and Isaia 2019). We
found two specimens in the olive orchard with EPM and that is the first recorded for the

16 Andelié Dmitrovié B et al

mainland. It used to be erroneously listed as a Central European species, but now it is
considered to be a Mediterranean one (Jantscher 2001).

Zodarion elegans (Simon, 1873) (Araneae, Zodariidae)

Z. elegans has a Mediterranean distribution (Nentwig 2022) and was recorded for Croatian
by Gasperini (1891). Since then, its presence was noted in Istria, Kvarner, including the Krk
Island and Dalmatia Region (Bosmans 1997). We sampled this species in both olive
orchards and in vineyards with EPM.

Ceratinella brevipes (Westring, 1851) (Araneae, Linyphiidae)

Ceratinella brevipes is a species of global distribution and records exist for all Croatia’s
neighbouring countries (Komnenov 2010, Nentwig 2022), so its presence was expected. In
this study, the species was sampled in olive orchards and vineyards with IPM. This is a
new record for Croatian fauna.

Class Insecta

Two carabid endemic species from this study with the area limited to the Balkan Peninsula
belong to the genus Carabus. The Balkan Peninsula is considered a taxon-rich region and
the hyper-diverse genus Carabus is present in this region with many endemics and
endangered species (Seri¢ Jelaska et al. 2014). In Croatia, thirty species of the genus
Carabus have been identified, including 53 subspecies (JambroSic Vladic et al. 2019). Like
spiders, carabid beetles are essential predatory arthropods in agricultural lands (Seri¢
Jelaska et al. 2014, Serié Jelaska and Symondson 2016), whose richness and diversity
promote biocontrol (Seri¢ Jelaska et al. 2022b). In this study, the IPM system resulted in a
higher diversity of carabids than the EPM which is opposite to findings for spiders. The
explanation is similar to that in the case of gastropods: Carabids are mainly ground active
and juveniles develop in the soil and, thus, could be under the direct influence of soil
treatments. This impact of soil disturbances by mechanical methods applied in agricultural
sites on the diversity of some groups like carabids has been already confirmed (Kromp
1999).

All three orthopteran endemics belong to the family Tettigoniidae (Bush crickets), which are
the largest orthopteran group in Croatia (Skejo et al. 2018). About 20% of bush crickets
fauna in Croatia is made of Balkan endemics and stenoendemics, which is due to the
physical barriers in the landscape (e.g. Dinaric Alps), variable habitats and for the fact that
numerous glacial microrefugia existed in the past (Kenyeres et al. 2009, Skejo et al. 2018).
In addition, for many Orthoptera species, their status in the IUCN list is described as data
deficient, amongst them Paramogoplistes novaki (Krauss, 1888). The first record of this
species was on the island of Hvar (Dalmatia, Croatia) at the close of the 19'" century. Since
then, several findings of the species were recorded in Croatia as follows: Hvar Island,
Neretva River Mouth, Mljet Island and Krka River (Skejo et al. 2018). As a part of our
research, P novaki was recorded in an olive orchard with EPM and this represents the
most northern record of this species so far and, thus, contributes to the knowledge of the
distribution of this rare species. The distribution of this species in Europe, other than

Mediterranean vineyards and olive groves in Croatia harbour some rare and ... 17

localities in Croatia, includes Greece and Italy (Lazio Region and Sardinia) (Hochkirch
2016).

Ditomus calydonius P. Rossi, 1790 (Coleoptera, Carabidae)

In the case of carabid beetles, notable was the record of the critically-endangered species
D. calydonius (Vujcic-Karlo et al. 2007). D. calydonius needs warms soil to develop
(Brandmayr and Brandmayr Zetto 1974). It combines summer aestivation with egg
deposition and brood care in the nest, where it collects seeds for larvae to feed on
(Brandmayr and Brandmayr Zetto 1974). This record emphasises the fact that agricultural
areas could be habitats for rare and endangered species and that it is of high importance
to adjust the management type to be more supporting of invertebrate’s diversity (Happe et
al. 2019). D. calydonius is an endangered and rare faunistic record.

Carabus caelatus dalmatinus Duftschmid, 1812 (Coleoptera, Carabidae)

Carabus caelatus Fabricius 1801 is a species native to the Alps, Dinarides and western
Balkans, with a distribution that spans the Dinaric Mountains (Jambrogié Vladié and Seri¢
Jelaska 2020). We sampled the subspecies Carabus caelatus dalmatinus in an olive
orchard with EPM that is located near the foothills of the Velebit Mountain. C. caelatus
dalmatinus, common name Dalmatian crimpled ground beetle, is noted in Albania, Croatia
and Bosnia and Herzegovina (Lob! and Lob! 2017). The adults are active from May to
August (JambroSsic Vladic¢ 2020). It is listed as Near threatened in the Red List of Carabid
beetles in Croatia, meaning they are not threatened yet, but there is a reasonable concern
that they might become in the future (Vujcic-Karlo et al. 2007).

Carabus coriaceus dalmaticus Géhin, 1885 (Coleoptera, Carabidae)

C. coriaceus is widely distributed in Europe (GBIF org. 2022) and subspecies C. coriaceus
dalmaticus can be found in Croatia, Albania, North Macedonia and Greece (Zicha 2015). It
is characterised by smoother elytrae and broader posterior lobes compared to the
nominate subspecies C. coriaceus coriaceus (Goidanich 1932). It was collected on all
sampling sites.

Amara dalmatina Dejean, 1828 (Coleoptera, Carabidae)

Amara dalmatina (Eng. Dalmatian shiny channel runner) is endemic to the Mediterranean
Region (Vigna Taglianti 2013). In this study, it was sampled in olive orchards with EPM and
these samples, along with their genetic data, are the first entries for this species in the
BOLD database (BOLD:AEN2004) (Ratnasingham and Hebert 2013).

Zabrus incrassatus (Ahrens, 1814) (Coleoptera, Carabidae)

This herbivorous carabid species is endemic to the Balkan Peninsula (Vigna Taglianti 2013
, leofilova 2020). In Croatia, it has been sampled at Neretva Delta (Kurbalija 2012) and
several localities in Dalmatia (Hvar, Split, Zadar) (Anichtchenko and Guéorguiev 2009). In
this study, it was sampled in olive orchards with EPM.

18 Andelié Dmitrovié B et al

Olistophus fuscatus Dejean, 1928 (Coleoptera, Carabidae)

There are five species of genus Olistophus in Europe and they prefer dry habitats on sandy
or limy soils (Trautner and Geigenmuller 1987). O. fuscatus has a Mediterranean
distribution and, while it is not listed in Red List of Carabid beetles in Croatia (Vujcic-Karlo
et al. 2007), it is considered to be a rare faunistically (Seri¢ Jelaska and Temunovié 2010).
In this study, it was collected in olive orchards with EPM and nearby unmanaged sites.

Latissus dilatatus (Fourcroy, 1785) (Hemiptera, Issidae)

L. dilatatus is a type species, by original designation and monotypy, of its genus, which has
a Mediterranean distribution (together with Hungary) (Bourgoin and T 2022). It was
recorded in Croatia for the first time by Melichar (1906).

Aphaenogaster picena Baroni Urbani, 1971 (Hymenoptera, Formicidae)

Aphaenogaster picena, endemic to the region of the Dinaric Alps, has only one previous
record for Croatia according to www.antweb.org (California Academy of Science 2002,
accessed on 21 March 2022). It is widely distributed in Italy, Slovenia and Albania (Boer
2013). This species prefers open fields with little vegetation, like all members of the
Aphaenogaster group. The first record for this species in Croatia was in Pakostane, Zadar
County (California Academy of Science 2002, accessed on 21 March 2022). In this study, it
was recorded in olive orchards with EPM.

Ephippiger discoidalis Fieber, 1853 (Orthoptera, Tettigoniidae)

E. discoidalis has a distribution range that encompasses zones from Greece to northern
Italy (Skejo et al. 2018). In Croatia, it is a common species in a Mediterranean area and it
inhabits parts of the Dinaric Alps as well, but only those areaswith a dominant
Mediterranean influence (Skejo et al. 2018).

Eupholidoptera schmidti (Fieber, 1861) (Orthoptera, Tettigoniidae)

E. schmidti occurs in the Western Balkan Peninsula, from northern Greece in the south, to
western Bulgaria, up to northern Italy (Hochkirch 2016, Skejo et al. 2018). It is a medium-
sized species, previously considered as a subspecies of E. chabrieri, but molecular
phylogenetic analysis confirmed its species status (Allegrucci et al. 2014).

Barbitistes yersini Brunner von Wattenwyl, 1878 (Orthoptera, Tettigoniidae)

B. yersini is a thermophilic species present in the Mediterranean part of Croatia as well as
in southern part of the Dinaric karst (Hochkirch 2016, Skejo et al. 2018). In Europe, it has
distribution that includes the Western Balkans and part of central Italy (Hochkirch 2016,
Skejo et al. 2018).

Mediterranean vineyards and olive groves in Croatia harbour some rare and ... 19

Aphthona pallida (Bach, 1856) (Coleoptera, Chrysomelidae)

The Coleopteran species of genus Aphthona can be used in biocontrol against weeds, but
some species may also cause economic damage on cultivated plants (Ozdikmen et al.
2018). The species is widely distributed in Europe (Vigna Taglianti 2013, GBIF org. 2022).
In this study, it was recorded in olive orchards with EPM. This is a new record for Croatian
fauna.

Anthomyia liturata (Robineau-Desvoidy, 1830) (Diptera, Tabanidae)

The A. /iturata group is most likely an opportunistic species, with larvae that can develop in
a wide variety of organic materials (Suwa and Darvas 1998, Pintilioaie et al. 2021). This
species is found throughout Europe; however, its small size makes identification difficult.
The first record of this species was obtained in vineyards with IPM using the DNA
barcoding method as a part of the MEDITERATRI project (Andelic Dmitrovic et al. 2022).
This is a new record for Croatian fauna.

Corynoptera perpusilla Winnertz, 1867 (Diptera, Sciaridae)

Winnertz (1867) established the genus Corynoptera for four new species, one of which, C.
perpusilla, was later chosen as the type species by Enderlein in 1911 (Hippa et al. 2010).
Hippa et al. (2010) reported Corynoptera perpusilla in Croatia’s neighbouring countries.
Species from the genus Corynoptera are often examples of the cryptic diversity (Moriniere
et al. 2019). There is a higher prevalence of unrecorded and ignored species in families
with the lowest body sizes, implying that the number of dipteran species in Croatia is likely
to be substantially larger than previously reported and, thus, new records are not surprising
(Moriniére et al. 2019, Andeli¢c Dmitrovic et al. 2022). This genus belongs to the family
Sciaridae. Sciaridae, commonly known as Dark wing fungus gnats, are a globally common,
but poorly researched dipteran family (Evenhuis et al. 2016), since their small size and
superficial homogeneity do not make them attractive to taxonomists and collectors. The
first record of this species for Croatian fauna was obtained in olive orchards with IPM using
the DNA barcoding method as a part of the MEDITERATRI project (Andeli¢ Dmitrovic et al.
2022). Findings such as this one underline the advantages of molecular tools in species
identification, such as the DNA barcoding method (Andelic Dmitrovic et al. 2022, Chimeno
et al. 2022).

Psilopa obscuripes Loew, 1860 (Diptera, Ephydridae)

The distribution of this species encompasses European countries: Austria, Bulgaria, the
Czech Republic, France, Germany, Greece, Spain and Turkey and North America (Mathis
and Zatwarnicki 2010). The first record of this species for Croatian fauna was obtained in a
vineyard with IPM using the DNA barcoding method (Andelic Dmitrovic et al. 2022), done
as part of the MEDITERATRI project. The flies of this family are often small and this
negatively affects their determination.

20 Andelié Dmitrovié B et al

Conclusions

We confirmed that endemic and rare species are present in agricultural areas of the
Mediterranean part of Croatia supporting the importance of agricultural land in preserving
and promoting biodiversity. Rare and endemic species were found under both EPM and
IPM management systems, showcasing the positive impact of these closer-to-nature
management types. Additional research on regional biodiversity in agricultural landscapes
is necessary especially having in mind several endangered species being recorded and
agriculture as one of the main drivers for biodiversity decline. Additionally, the first records
we had for the area justify the need of further biodiversity assessments, in which
agricultural sites should be included.

Acknowledgements

We are grateful to Josip Skejo for his contribution in identifying Orthoptera specimens and
Josip Primorac for sorting field samples with ants, as well to professor Stjepan Krcmar, for
offering his knowledge on dipteran species and their distribution. We are thankful to all the
students and associates who helped with the feldwork and samples preparation. We are
also thankful to the owners of olive orchards and vineyards, Miodrag DeSa, Josip Razov
and Sime Skaulj in Zadar County who kindly let us conduct our research on their land. This
research was funded by The Croatian Science Foundation under the MEDITERATRI
Project (HRZZ UIP 05-2017-1046) granted to Lucija Seri¢ Jelaska and co-funded by the
Department of Biology, Faculty of Science at the University of Zagreb. We are also thankful
to the Croatian Academy of Sciences and Art (HAZU) for co-funding the research within the
Croatian CryoEntoArk project (project number 10-102/324-247-2021).

Grant title

Neonicotinoids and Copper in the Mediterranean Agriculture — their effects on non-target
invertebrates (MEDITERATRI Project (HRZZ UIP 05-2017-1046)).

Krio EntoArka — barkodiranje i pohrana DNA i tkiva ugrozenih i zasticenih kukaca u
Hrvatskoj (10-102/324-247-2021).

Hosting institution

Department of Biology, Faculty of Science at the University of Zagreb.

Conflicts of interest

The authors have declared that no competing interests exist.

Mediterranean vineyards and olive groves in Croatia harbour some rare and ... 21

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Supplementary materials

Suppl. material 1: Supplementary figure 1 EJ

Authors: MEDITERATRI project team

Data type: Image

Brief description: Figure of Ceratinella brevipes (A) dorsal view; (B) dorsal view of pedipalp; (C)
ventral view of pedipalp.

Download file (39.18 kb)

Suppl. material 2: Supplementary figure 2 [5

Authors: MEDITERATRI project team

Data type: Image

Brief description: Lateral view of Anthomya liturata.
Download file (26.06 kb)

Suppl. material 3: Supplementary figure 3 EE)

Authors: MEDITERATRI project team

Data type: Image

Brief description: Lateral view of Corynoptera perpusilla.
Download file (18.09 kb)

Suppl. material 4: Supplementary figure 4 [I

Authors: MEDITERATRI project team

Data type: Image

Brief description: Lateral view of Psilopa obscuripes.
Download file (20.30 kb)